Behav Ecol Sociobiol (2008) 63:123–133
DOI 10.1007/s00265-008-0642-0
ORIGINAL PAPER
The behavioral ecology of cannibalism in cane toads (Bufo
marinus)
Lígia Pizzatto & Richard Shine
Received: 15 November 2007 / Revised: 18 July 2008 / Accepted: 18 July 2008 / Published online: 8 August 2008
# Springer-Verlag 2008
Abstract Laboratory studies show that predatory cane
toads (Bufo marinus) exhibit specialized toe-luring behavior that attracts smaller conspecifics, but field surveys of
toad diet rarely record cannibalism. Our data resolve this
paradox, showing that cannibalism is common under
specific ecological conditions. In the wet–dry tropics of
Australia, desiccation risk constrains recently metamorphosed toads to the edges of the natal pond. Juvenile toads
large enough to consume their smaller conspecifics switch
to a primarily cannibalistic diet (67% of prey biomass in
stomachs of larger toads). Cannibalistic attack was triggered by prey movement, and (perhaps as an adaptive
response to this threat) small (edible-sized) toads were
virtually immobile at night (when cannibals were active).
Smaller metamorphs were consumed more frequently than
were larger conspecifics. The switch from insectivory to
cannibalism reflects the high dry season densities of small
conspecifics (in turn, due to desiccation-imposed constraints to dispersal) and the scarcity of alternative (insect)
prey during dry weather. Our study pond (102 m in
circumference) supported >400 juvenile toads, which
consumed many metamorphs over the course of our study.
Toads appear to be low-quality food items for other toads;
in laboratory trials, juvenile toads that fed only on
conspecifics grew less rapidly than those that ate an
equivalent mass of insects. This effect was not due to
parotoid gland toxins per se. Thus, cane toads switch to
intensive cannibalism only when seasonal precipitation
Communicated by J. Christensen - Dalsgaard
L. Pizzatto : R. Shine (*)
School of Biological Sciences A08, University of Sydney,
Sydney, New South Wales 2006, Australia
e-mail: [email protected]
regimes increase encounter rates between large and small
toads, while simultaneously reducing the availability of
alternative prey.
Keywords Anuran . Feeding habits . Growth rate .
Intraspecific predation . Natural selection
Introduction
“I do wish we could chat longer, but I’m having an old
friend for dinner”—Dr. Hannibal Lecter, in “The
Silence of the Lambs”
Cannibalism is widespread among living creatures (Fox
1975; Polis 1981), ranging from unicellular organisms
(Claverys and Havarstein 2007) to humans (Shankman
1969). Eating conspecifics may enhance the cannibal’s
fitness via direct nutritional benefit (Fox 1975; Polis 1981;
Ebensperger 1998; Manica 2002; Lourdais et al. 2005) or
via less direct pathways (Polis 1981; Summers 1989;
Forster 1992; Sasaki and Iwahashi 1995; Andrade 1996,
1998). In amphibians, cannibalism is common in early life
history stages (Crump 1992; Rosen 2007). The larvae of
some species exhibit discrete morphs that differ in feeding
habits and associated trophic morphologies, with one morph
acting as specialized cannibals (Collins and Holomuzki
1984; Crump 1992; Larson et al. 1999). Predation by tadpoles upon freshly laid eggs is so common as to be the
norm rather than the exception (Crump 1992; Duellman and
Trueb 1994; Alford 1999), and the most significant
predators of tadpoles may be other amphibians (Duellman
and Trueb 1994), perhaps facilitating conspecific predation.
However, less is known about cannibalism in the terrestrial
phase of the anuran life cycle (Crump 1992; Wiseman and
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Bettaso 2007). Many frogs and toads are generalized
feeders (Toft 1985) so that other anurans (including conspecifics) are likely to be consumed occasionally (Crump
1992; Alford 1999). Some frog species are specialized to
prey upon other frogs (Duellman and Trueb 1994), and
cannibalism may be more common in such taxa (see Scott
and Aquino 2005 for evidence that conspecific predation
may be rare in such an assemblage, although cannibalism
was easily induced by experimental presentation of smaller
conspecifics to foraging adults). Nonetheless, despite many
anecdotal reports of cannibalism among non-larval anurans,
we are not aware of any detailed analyses of this topic.
Recent work suggests a potential model system for such
a study. One of the most intensively studied anurans
worldwide is the cane toad Bufo marinus; for example, a
recent 230-page book was devoted to reviewing published
literature on this species (Lever 2001). Extensive dietary
data (based on stomach contents of field-collected specimens) show that adult cane toads take a wide range of prey
items but with a strong preponderance of small invertebrates (see Lever 2001 for a review). Such studies come
from the native range of cane toads in South America (Zug
and Zug 1979; Bayliss 1995) as well as countries to which
the toad has been introduced (e.g., continental USA—Pack
1922; Hawaii—Illingworth 1941; Oliver and Shaw 1953;
Puerto Rico—Box 1925; Dexter 1932; Fiji—Hinckley
1963; Papua New Guinea—Pippet 1975; Zug et al. 1975;
Bailey 1976; Australia—Niven and Stewart 1982; Freeland
et al. 1986; Greenlees et al. 2006). Hence, despite
occasional reports of predation on vertebrates, including
other frogs (Covacevich and Archer 1975; Quesnel 1986;
Bayliss 1995; Caudell et al. 2000), and a single record of
two juveniles being eaten by conspecifics (Zug et al. 1975),
the cane toad at first sight seems an unlikely candidate for a
study on cannibalism. However, recent detailed observations on captive cane toads revealed a complex, stereotyped
toe-luring behavior that was performed primarily by
medium-sized toads, was stimulated by the proximity of
smaller (edible-sized) conspecifics, and elicited close
approach by those smaller animals (Hagman and Shine
2008). Experimental manipulation of toe colors and
movement frequencies showed that the lure was well-suited
to attract smaller conspecifics and, hence, appears to be an
adaptation for cannibalism (Hagman and Shine 2008).
These results seem paradoxical in light of field reports that
anurophagy is rare in cane toads (see above). One
resolution of this paradox might be that cannibalism is
indeed an important part of toad trophic ecology but only
under specific ecological conditions.
In the course of field studies on cane toads near the
invasion front in tropical Australia (Brown et al. 2006;
Phillips et al. 2007), we identified a situation that might
Behav Ecol Sociobiol (2008) 63:123–133
facilitate cannibalism. During the prolonged dry season
(April to November), toads breed sporadically, but desiccation risk in the surrounding landscape constrains metamorph and small toads (but not adults—see “Discussion”)
to the moist margins of the natal pond (Child et al. 2008;
see also Freeland and Kerin 1991; Cohen and Alford 1993,
for studies in other areas). The consequent high densities of
small metamorphs provide an opportunity for predation by
larger juvenile conspecifics, especially because dry weather
reduces the availability of alternative (invertebrate) prey
(Child et al. 2008). We, thus, conducted detailed studies of
one such pond, to ask:
(1) Do juvenile toads in this situation act as specialist
cannibals?
(2) Could the risk of cannibalism explain why small
metamorphs are active diurnally, unlike their older
conspecifics which are nocturnally active?
(3) Does cannibalism substantially affect population demography or the growth rates of larger toads?
Materials and methods
Study species
The cane toad B. marinus (= tentatively allocated to Chaunus
marinus by Frost et al. 2006) is a large [to 24-cm snouturostyle length (SUL), 2.8 kg] terrestrial anuran native to
South and Central America but widely translocated
elsewhere in attempts to control insect pests affecting
agricultural enterprises (Lever 2001). Cane toads were
brought to Queensland in 1935 and are now abundant
throughout most of tropical Australia (Urban et al. 2007). In
the wet–dry tropics of the Northern Territory, toads breed
sporadically over much of the year but with a peak in the
late wet season and early dry season (March–June: R.
Shine, unpublished data). Because a single clutch can
contain >30,000 eggs, transforming metamorphs can attain
high densities at water body margins during the dry season
(Freeland and Kerin 1991; Cohen and Alford 1993; Child et
al. 2008). Metamorph toads are primarily diurnal, whereas
larger juveniles and adults are nocturnal (Freeland and
Kerin 1991; Child et al. 2008; Pizzatto et al. 2008).
Study area
We worked at a circular pond (approximately 2 m deep;
circumference 101.7 m) beside the Arnhem Highway, about
70 km east of Darwin (12°39′36.46″ S, 131°20′11.28″ E).
The pond was lined by open muddy banks 10–60 cm wide,
flanked on the edge by thick grass (Fig. 1a). In July 2007,
Behav Ecol Sociobiol (2008) 63:123–133
125
Fig. 1 In the mid-dry season
(July), the margins of the natal
pond (a) provide the only moist
microhabitats within the nearby
landscape. Hence, both newly
metamorphosed cane toads and
larger, older conspecific juvenile
toads were concentrated on
these pond margins (b). Juvenile
toads readily seized metamorphs
dangled in front of them (c),
and dissection of juveniles
revealed that cannibalism
was frequent (d)
the pond contained many fishes (e.g. Melatotaenia australis, Mogurnda mogurnda, Oxyeleotris lineolata, Glossamia aprion, Amniataba percoides, Megalopes cyprinoides),
anurans (Litoria bicolor, Litoria dahlii, Litoria microbelos,
Litoria nasuta) and one saltwater crocodile (Crocodylus
porosus). Cane toads bred in the pool on multiple occasions
from the mid-wet season (first record of amplexus 13
December: M. Crossland, personal communication)
through the early dry season (June) and tadpoles continued
to metamorphose and emerge from the water during our
studies in July. At this time, the toads around the pond fell
unambiguously into three size classes: newly emerged
metamorphs (<20 mm SUL), juveniles (20–70 mm), and
adults (>70 mm), with no intermediate-sized animals. The
muddy banks of the pond contained high densities of
metamorphs (25 to 145 m 2, based on quadrat counts)
whenever we checked, by day or night, whereas larger
(juvenile and adult) toads were seen only at night (Fig. 1b).
Juvenile toads were seen emerging in the early evening
from holes under rocks and from grassy retreats.
Dietary habits and estimating densities of cannibals
and their prey
The massive numbers of metamorphs emerging from the
pond, and the prolonged period over which they did so,
precluded direct enumeration. However, we estimated (1)
the relative numbers of small metamorphs and juvenile
toads in 18 quadrats along the bank (each 100×20 cm) and
(2) the total number of toads in the juvenile size class. To
assess the latter variable, the larger (juvenile) animals were
repeatedly sampled (with removal) on 33 nights over a
5-week period from 12 June to 22 July 2007. A random
subsample of 41 of these animals was euthanized within an
hour of collection (first anesthetized by immersion in
tricaine methanesulfonate [MS222] then killed by freezing)
and dissected to score their stomach contents. The remaining 378 juvenile toads (i.e., those not euthanized immediately after capture) were kept for use in other experiments.
We also took random samples of metamorphs on two of
those nights, to quantify body size distributions.
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Spontaneous activity and response to disturbance
To quantify nocturnal–diurnal shifts in behavior of metamorph toads, we haphazardly selected the first individual
we saw when we carefully approached the pond edge (to
within 1 m of the water) and scored whether or not they
moved over a 2-min period. To assess their response to a
predation threat, we touched each metamorph on the back
with a twig and recorded whether the animal remained
immobile or moved away. These experiments were run
during the day (1600 to 1700 hours) and night (2000 to
2100 hours) on consecutive days.
Cues for cannibalistic attack
Would immobility protect metamorph toads from cannibalistic attack? It is well known that prey movement can elicit
a feeding response by toads (e.g., Buxbaum-Conradi and
Ewert 1999), but prey odor, without movement, can also
elicit feeding (Dole et al. 1981; Roth and Wiggers 1983).
Indeed, cane toads are renowned for taking nonmoving
prey such as dog food (Lever 2001). Ten metamorph toads
(collected as part of the random sampling to document
metamorph size distributions: see above) were anesthetized
by immersion in tricaine methanesulfonate and then killed
by freezing. We then thawed these animals and used them
as lures to investigate feeding responses of larger toads
(Fig. 1c). Metamorphs were suspended on cotton thread
from fishing rods for these trials, and all observations were
made in the field under red light and for 2-min periods.
Trials were conducted from 1930 to 2130 hours. We
manipulated two variables: metamorph body size (“small” =
11–12.5 mm; “large” = 14–16 mm) and movement
(“immobile” = metamorph deposited on substratum 1 cm
in front of the snout of a juvenile toad; “moving” =
metamorph moved about similarly to natural activity in
front of the larger toad). Treatments were applied in random
order, and we scored whether or not each juvenile toad
seized the metamorph. All juvenile toads were then
collected and euthanized as above.
Effects of cannibalism on growth rates
We investigated the influence of cannibalism on predator
growth by keeping juvenile toads (1.2–3.77 g) individually
in plastic containers (15×10×7 cm) lined with wet sand
and with ad libitum access to water in a shaded outdoor
area (and, thus, exposed to natural air temperatures and
photoperiod). All containers included a cardboard shelter
attached to the side of the container to provide refuge.
Twelve juvenile toads were fed on smaller metamorph
toads only (maintained during the trials in containers
identical to those used for larger toads, but in groups of
Behav Ecol Sociobiol (2008) 63:123–133
20 per container; fed on tiny crickets), and 15 were fed on
crickets only. The juvenile toads were allowed to feed ad
libitum by introducing metamorphs or crickets to each cage
at night and removing uneaten animals the following
morning (which were then returned to their home cages).
Metamorphs do not feed at night (Pizzatto et al. 2008) so no
prey items for this size class were added during these
nocturnal trials. All prey items provided to the juvenile
toads (i.e., crickets or metamorph toads) were preweighed
(to 0.01 g). Juvenile toads were weighed at the outset of the
study, fed for 12 days and then reweighed. All animals
(juveniles and surviving metamorphs) were then euthanized
as above. Because this experiment provided a surprising
result (see below), we repeated it to compare growth rates
of juvenile toads fed either on crickets (as above) or on
crickets painted with the parotoid gland secretions of toads.
We obtained the toxin by manually squeezing the parotoid
glands of recently killed adult toads, to provide several
times more toxin per cricket (approximately 0.01 g) than is
found within the parotoid glands of a metamorph toad. We
fed 14 juvenile toads (5.3–12.5 g) on crickets and 12 toads
on crickets painted with toad toxin.
Results
Stomach contents analysis
Of seven large adult toads (>95 mm SUL, 70 g) collected at
the pond, five had empty stomachs, one contained an ant,
and one a beetle. Of the 124 juvenile toads that we
dissected, 29 had empty stomachs (chi-square test testing
null hypothesis of equal % empty stomachs adults vs.
juveniles, χ2 =5.67, df=1, P<0.02). The 95 juveniles with
food contained a total of 443 prey items, of which 69
(15.5%) were metamorph toads (Fig. 1d). Although a
minority numerically, these metamorphs constituted two
thirds of the total biomass of prey recorded in stomachs of
juvenile toads (13.08 of 19.44 g). Non-anuran prey items
were invertebrates, mostly ants (186 items, 1.72 g), beetles
(115 items, 1.69 g), and hemipterans (35 items, 2.22 g),
plus a few arachnids (5, 0.19 g), orthopterans (2, 0.47 g),
and dipterans (2, 0.07 g). The body size of a juvenile toad
was not significantly correlated with that of its prey (linear
regression using mean prey size per predator, n= 41
predators, r=0.15, P=0.35 for prey SUL; n=39, r=0.20,
P=0.23 for prey mass). The metamorphs consumed by
juvenile toads were smaller on average than those in the
random samples of surviving metamorphs in terms of body
length [analysis of variance (ANOVA): SUL, F1,821 =8.29,
P=0.004; Fig. 2] but not body mass (ANOVA: F1,821 =0.67,
P=0.42). This minor bias was probably due to reduced
vulnerability of the (infrequent) larger metamorphs (Fig. 2).
Behav Ecol Sociobiol (2008) 63:123–133
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progress (smaller toads in the mouths of larger conspecifics) during our nocturnal surveys, so most identifiable
anuran prey items in stomachs probably were consumed in
the few hours prior to our surveys.
Densities of cannibals and their prey
Our quadrat counts conducted within 2 h of dusk revealed
average densities of 54.2 (SD=32.50, range 25 to 145)
metamorph toads and 2.9 (SD=3.45) juvenile toads per
square meter, respectively (see Fig. 1b). Because metamorphs (mean mass 0.23 g) were about 20 times as
common as their larger conspecifics (mean mass 7.8 g),
the total standing-crop biomass of the two groups was fairly
similar. Mean metamorph densities did not differ significantly between quadrats that contained or did not contain
cannibalistic juvenile toads (ANOVA: F1,17 =2.23, P=0.15).
Although we never found more than 49 juvenile toads on
any single night, new individuals kept appearing to replace
the ones we had removed; in total, we collected and
removed a total of 419 juveniles and seven adults from the
pond margins over 33 nights, and doubtlessly failed to find
many others.
Spontaneous activity and response to disturbance
When observed during daylight hours, 81% of metamorphs
(34 of 42) changed their locations during the 2-min
observation period. At night, spontaneous activity was seen
in only 14% of animals (chi-square test: 6 of 42; comparing
day vs. night, χ2 =33.08, df=1, P<0.0001). When touched
with a twig during daylight hours, 59% of metamorphs
moved away, compared to 12% at night (chi-square test: 33
of 56 vs. 7 of 60; χ2 =26.58, df=1, P<0.0001).
Cues for cannibalistic attack
Fig. 2 Body sizes of recently emerged metamorph cane toads and of
the larger juvenile conspecifics that preyed upon them. The upper
graph (a) shows the frequency distribution of body sizes of the sample
of 780 surviving metamorph toads; the middle graph (b) shows the
sizes of 67 metamorph toads found in the stomachs of cannibalistic
conspecifics; and the lower graph (c) shows the body sizes of 124
juvenile (putative cannibal) toads. Note the different scales on axes for
metamorph versus juvenile toads
Most of the prey items that we identified were freshly
ingested; metamorph toads in the stomachs of juveniles are
barely recognizable 24 h after ingestion (L. Pizzatto,
unpublished data). We saw three cases of cannibalism in
Juvenile toads never attacked immobile metamorphs, but
seized 45% of moving “lures” (chi-square test: 0 of 15 vs.
17 of 38; χ2 =7.97, df=1, P<0.005). The size of the
metamorph used as a “lure” did not influence the predators’
responses (chi-square test: attacks in eight of 19 trials with
“small” lure, nine of 19 trials with “large” lure; χ2 =0.00,
df=1, P>0.99).
Effects of cannibalism on growth rates
In the first experiment, both groups of juvenile toads
increased significantly in mean body mass over the trial
period (comparing initial vs. final mass with paired t-tests;
cannibals, t=0.86, df=11, P<0.0001; insectivores, t=1.83,
df=14, P<0.0001). The toads that fed on conspecifics grew
less rapidly than those that ate an equivalent mass of
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crickets, however [analysis of covariance (ANCOVA) with
prey mass ingested as the covariate, mass gain as the
dependent variable: slopes homogeneous so interaction
term deleted; main effect of diet, F1,24 =9.80, P<0.005;
see Fig. 3]. When we repeated the trials to compare growth
rates of toads that were fed crickets with or without
parotoid gland secretions, growth rates were unaffected by
toxin addition (ANCOVA with prey mass ingested as the
covariate, mass gain as the dependent variable: slopes
homogeneous so interaction term deleted, main effect of
diet, F1,23 =0.54, P=0.47).
Discussion
Extensive published analyses of dietary habits show that
adult cane toads feed primarily on invertebrate prey,
typically small ants, termites, and beetles (Zug et al.
1975; Zug and Zug 1979; Bayliss 1995; Lever 2001). This
conclusion is consistent with our limited data on adult toads
from the study pond, as well as extensive information from
nearby study sites (Greenlees et al. 2006; M. Greenlees,
unpublished data). Recently emerged metamorph toads also
feed exclusively on tiny invertebrates (Child 2007; T.
Child, unpublished data). In striking contrast, however,
our data show that intermediate-sized (juvenile) toads
function as specialist cannibals under some circumstances,
with about two thirds of their prey biomass consisting of
Fig. 3 Growth increments of captive cane toads over a 12-day period
as a function of their diet. Twelve toads were fed entirely on juvenile
conspecifics, whereas 15 were given crickets. In both cases, food was
provided ad libitum; toads grew more rapidly on crickets than on a
cannibalistic diet
Behav Ecol Sociobiol (2008) 63:123–133
smaller toads. The population that we studied is an invasive
one, and we know relatively little about the ecological
parameters of natural populations of cane toads (Zug and
Zug 1979). However, the climate of our study area is
broadly similar to that over much of the toad’s natural range
(Lever 2001); hence, many of the same constraints and
opportunities are likely to occur. Many ecological aspects of
cannibalism in cane toads also display strong analogies with
cannibalism in other animal species, as discussed below.
First, body size plays a major role. Cannibalism appears
to be characteristic of juvenile cane toads, rather than adults
or metamorphs. Similar size-specificity of cannibalism is
widespread. Although typically the cannibals are the largest
individuals in the population (see Fox 1975; Polis 1981;
Crump 1992), as in bullfrogs (Korschgen and Moyle 1955;
Bury and Wheian 1984; Schwalbe and Rosen 1988; Stuart
1993; Rogers 1996), a greater incidence of cannibalistic
behavior in intermediate-sized individuals has been
reported for some fishes, dragonfly larvae, and parasitoid
insect larvae (see Polis 1981) as well as the cane toad
(present study); and there is one record of a young-of-theyear Rana pipens berlandieri with a conspecific in its
mouth (Kirn 1949). Similarly, the victims of cannibals are a
nonrandom subset of the population, typically the smallest
and/or weakest animals (see Polis 1981; Crump 1992). In
our cane toad population, the individuals that were eaten
were smaller, on average, than the survivors of the same
cohort; indeed, many of the animals consumed likely had
emerged from the water only recently. Although it is clear
that other life history stages of cane toads also engage in
cannibalism (e.g., tadpoles eat eggs, and large adults
consume smaller conspecifics: Zug et al. 1975; Lever
2001; M. Crossland, personal communication), predation
of juvenile animals upon recent metamorphs is the most
common such interaction. Why are these particular age or
size groups involved? The likely explanations are that:
(1) Newly metamorphosed anurans have limited locomotor abilities and may be especially vulnerable to
predation at this time (Wassersug and Sperry 1977;
Huey 1980). In at least four species of spadefoot toads
(genera Scaphiopus and Spea) and in the treefrog
Osteopilus septentrionalis, younger conspecifics cannibalize transforming individuals (Bragg 1964; Crump
1986, 1992; Alford 1999);
(2) These small animals occur at high densities and are
accessible because they do not hide in refuges at night
when larger conspecifics are active; and
(3) Desiccation risk restricts these two groups (metamorphs
and juveniles) to pond margins during the dry season,
whereas larger adult toads can disperse into food-rich
areas further from water (Freeland and Kerin 1991;
Cohen and Alford 1993; Child et al. 2008).
Behav Ecol Sociobiol (2008) 63:123–133
Hence, encounter rates between adult toads and smaller
(edible-sized) conspecifics will be much lower than
between metamorphs and juveniles; adult toads were rarely
seen during our study and those at the pond appeared to be
there for rehydration or breeding rather than for feeding
(based on their mostly empty stomachs).
The dynamics of cannibalism in cane toads likely
depend upon seasonal schedules of precipitation and, thus,
toad recruitment and dispersal. The cannibals in our study
were toads that had emerged from this same (isolated)
waterbody a few months previously, from clutches laid
earlier in the wet season (based on growth rates measured
in toads at a nearby site: G. P. Brown, personal communication), thus cannibals and metamorphs are unlikely to be
siblings. Hence, the prolonged breeding season of toads is
critical in that it generates sufficient disparity in ages (and,
thus, body sizes) of small toads around a waterbody to
enable some individuals to grow large enough to consume
others. If breeding was highly synchronized, or if metamorph toads could disperse from the waterbody margins
soon after they emerged from the water, cannibalism would
be less common; explosive (synchronous) breeding
decreases intraspecific predation in Rana sylvatica (Petranka
and Thomas 1995). Cane toad metamorphs do indeed
disperse soon after emergence during the wet season, when
the risk of desiccation is virtually eliminated by frequent
rain and luxuriant vegetation cover (Child et al. 2008).
Thus, the high incidence of cannibalism may be a direct
result of the extreme seasonality in precipitation in the wet–
dry tropics, coupled with the extended breeding seasonality
of cane toads in this area. A similarly central role of
reproductive timing is seen in other cases of cannibalism:
for example, early-hatching beetles search for, and eat,
later-deposited eggs and younger larvae (Kaddou 1960;
Brown 1972) and poison-arrow frog tadpoles (Dendrobates
ventrimaculatus) cannibalize eggs laid later in the wet
season (Poelman and Dicke 2006) and, thus, as in B.
marinus, the cannibals are the early-hatching animals. The
incidence of cannibalism also depends on specific conditions in spadefoot tadpoles and larval salamanders.
Cannibal morphs of tiger salamanders grow faster than
non-cannibals and are more likely to develop in temporary
ponds than in permanent ponds (Pfennig 1997). In spadefoot tadpoles, older individuals sometimes are consumed by
younger ones (Bragg 1964). Two-legged and four-legged
tadpoles usually do not attack conspecifics (even younger
ones) in metamorphic aggregations; however, they will
promptly attack and eat newly emerged toadlets that fail to
leave the water (Bragg 1964).
The incidence of cannibalism (proportion of the diet
composed of conspecifics) often varies seasonally (Bulkley
1970; Chevalier 1973; Forney 1974), as it does in cane
toads. The proximate mechanisms generating seasonal
129
variation in the incidence of cannibalism vary among
species but often may involve seasonal concentration of
individuals around specific biotic or abiotic resources (as
occurs with toads). High population densities are a strong
correlate of cannibalism (see Fox 1975; Polis 1981; Collins
and Cheek 1983; Crump 1992), presumably because higher
densities provide more opportunities for encounters between conspecifics. Experimental studies show that encounter rates influence the frequency of cannibalism in a
range of taxa (Thibault 1974; Fox 1975; Polis 1981).
Seasonal depression of alternative food supplies (Fox 1975;
Polis 1981; Collins and Cheek 1983), especially of higher
quality food (Babbitt and Meshaka 2000), also may militate
towards cannibalism and may play a major role in cane
toads. Invertebrate biomass falls dramatically with drier
cooler conditions at the onset of the dry season, with a
concomitant decrease in food intake and body condition of
cane toads (G. P. Brown, personal communication).
Because the increasingly arid landscape prevents dispersal,
the end result is a concentration of increasingly hungry
juvenile toads with only one abundant food source: smaller
conspecifics.
In some amphibian species, cannibalistic habits typify
only a proportion of each cohort, with morphological and
behavioral correlates related to the ingestion of conspecifics
(reviewed by Polis and Myers 1985; Crump 1992). In some
other amphibians, however, all or nearly all individuals take
conspecifics as prey (e.g., Ambystoma tigrinum: Rose and
Armentrout 1976; Lannoo and Bachmann 1984; Holomuzki
1986); thus, conspecifics can comprise a high proportion of
prey taken by an entire cohort (e.g., in the frogs Rana
esculenta and Rana ridibunda, conspecific tadpoles and
smaller individuals comprise up to 20% of prey volume for
adults; Dushin 1975). Most or all juvenile cane toads
appear to function as cannibals. We can confidently score
willingness to consume conspecifics for the 38 juvenile
toads that we tested with “lures” of dead metamorphs. Of
these animals, 18 attacked the “lure” and nine of the
remainder contained freshly ingested toads in their stomachs. Thus, at least 27 of 38 juvenile toads (71%) acted as
cannibals if given the opportunity; we suspect that this
would have been true for all individuals if testing were
repeated. In our experience, virtually all captive cane toads
readily consume smaller conspecifics (L. Pizzatto and R.
Shine, personal observation).
In some amphibians, the high incidence of cannibalism
among larvae constitutes a major threat to siblings and may
have favored the evolution of kin discrimination (Pfennig
1999). For example, spadefoot tadpoles and larval tiger
salamanders prefer to consume nonkin conspecifics (Pfennig
1997; Pfennig et al. 1994), and the presence of siblings
suppresses the development of cannibalistic morphs (Pfennig
and Collins 1993; Pfennig and Frankino 1997). In our
130
system, cannibal cane toads and their prey differ considerably in size (and, thus, cohort identity); thus, the system is
unlikely to create a selective force for kin recognition
(Pfennig 1999). However, the high incidence of cannibalism may have imposed significant selection on the
behaviors of both potential cannibals and potential victims.
For example, toe-luring is most commonly exhibited by
medium-sized toads (the same size group identified as
cannibals in the present study) and functions to attract
edible-sized conspecifics (Hagman and Shine 2008). Similarly, the behavioral traits of metamorph toads may reduce
their vulnerability to predation. Most obviously, times of
activity differ ontogenetically: all size classes of cane toads
except the smallest animals are exclusively nocturnal
(Freeland and Kerin 1991). Metamorphs at our study site
were virtually immobile at night, even if touched, whereas
they were active by day. This response was driven by light
levels not temperatures because metamorph toads were
similarly immobile if placed under low illumination levels
at high temperatures (Pizzatto et al. 2008). Our experimental trials demonstrated that immobility offers an effective
defense against predatory conspecifics (as expected from
the movement-activated visual systems of toads; BuxbaumConradi and Ewert 1999). Ontogenetic shifts from diurnal
to nocturnal habits are seen in many species of toads (Bragg
1940; Bragg and Weese 1950; Cunningham 1962; Sievert
and Sievert 2005) and may reflect an adaptation to avoid
cannibalism in many or all of these taxa.
Cannibalism can have significant consequences at the
population level also (Fox 1975; Polis 1980). In extreme
cases, cannibalism may eliminate a large proportion of
offspring (>90% of chicks and eggs of crows; Yom-Tov
1974) or entire cohorts (see Fox 1975; Polis 1981). Even
very low rates of cannibalism can have significant effects
on a population (Chevalier 1973). We lack data on the
numbers of metamorphs emerging at our study pond, but
cannibalism at our study pond may be common enough to
significantly influence metamorph survival. We recorded an
average of 12 juvenile toads active per night; if each of
these animals took a single metamorph per night (as is
likely; we sampled early in the evening, so metamorphs
caught later in the night were not included in our stomach
contents data), then about 12 metamorphs would be
consumed each night, or 360 each month, and >1,440 over
the critical period in the early to mid-dry season. This
predation is imposed on the survivors of density-dependent
mortality processes that occur earlier in the life history
(Cohen and Alford 1993). The end result may be to reduce
total effective recruitment of cane toads from the natal pond
(if predation kills animals that would otherwise have
survived to disperse in the subsequent wet season) or to
increase recruitment (if the death of already-doomed
smaller metamorphs enhances survival prospects of a small
Behav Ecol Sociobiol (2008) 63:123–133
number of larger, older animals). Given widespread concerns about the ecological impact of cane toads in Australia
(Phillips and Shine 2005), the degree of density-dependence
in mortality rates warrants further study.
An intriguing consequence of one size class preying
upon a different size class is that juvenile toads obtain
nutrients that ultimately are derived from sources (parental
investment in egg yolk and tiny invertebrates consumed by
metamorphs) from which they would otherwise be unable
to extract any benefit. In that sense, cannibalism may
enable a population to persist by expanding the range of
food sources that it can acquire (the “Life Boat Strategy”;
Polis 1980, 1981). If juveniles take many emerging
metamorphs, the end result at a population level would be
a functional increase in offspring size—and given the very
small size of bufonid metamorphs (Cohen and Alford
1993), such an increase might well be favored under
circumstances of high desiccation risk (Child et al. 2008).
Cannibalism also enhances the survival advantages of
reproducing early in the season because it is progeny from
these early clutches that grow large enough to function as
cannibals later in the season (for similar examples, see
Anhold 1994; Kinoshita 1998; Matsushima and Kawata
2005). Several authors have speculated that cannibalism
also may benefit the predator by reducing the density of
competitors, but this issue is inapplicable to cane toads. The
size disparity between cannibals and their prey results in a
major divergence in the size of dietary items (mean lengths
1.3 vs. 12.9 mm; Child 2007; T. Child, unpublished data);
thus, removing small metamorphs is unlikely to enhance
feeding opportunities for larger toads. Lastly, cannibalism
might affect population demography by facilitating the
spread of parasites (Gajdusek and Alpers 1972; Matuschka
and Bannert 1989; Pfennig et al. 1998; Macneil et al. 2003).
Some Australian populations of cane toads are heavily
parasitized by nematode lungworms (Barton 1998) that can
be transferred by direct ingestion (Baker 1979; Smyth and
Smyth 1980), and this possibility merits further study
because of its potential relevance to toad control (Kelehear
2007).
Lastly, cannibalism can confer an energetic and nutritional benefit to the cannibal, such that cannibals grow
faster than their non-cannibal kin (Lannoo et al. 1989;
Crump 1992; Wildy et al. 1998). However, our data paint a
cautionary picture in this respect. The biomass of ingested
prey may be a poor guide to nutritional value in cane toads
because a given biomass of metamorphs supported less
bodily growth of the predator than did the same mass of
insects (crickets). Cannibalism does allow a juvenile toad to
grow but not to grow as rapidly as if it had access to
invertebrate prey. Similarly, low growth rates from consumption of toads (compared to frogs) have been reported
also for snakes that eat these anurans (Llewelyn et al.
Behav Ecol Sociobiol (2008) 63:123–133
2008). This result suggests that cane toads constitute poorquality food. The most obvious explanation would involve
the powerful toxins that they possess, but our second
growth-rate experiment suggests instead that the most
important factor may be nutritional content rather than
costs of detoxifying parotoid secretions. Further work is
needed to clarify this puzzling result.
In summary, cannibalism in cane toads is readily
interpretable in the light of this species’ ecology within
the wet–dry tropics. The seasonality of precipitation
regimes—and, thus, of the degree of aggregation of
metamorphs, the rates of encounter between metamorphs
and juvenile toads, and the availability of alternative
(insect) prey—ultimately may drive the incidence and
timing of cannibalism in this population. Thus, for
example, surveys during the wet season show no large
juvenile toads remaining near waterbodies; metamorph
toads disperse soon after emerging and rarely return to the
natal pond (Child et al. 2008). Cane toads appear to rely on
cannibalism only under circumstances where smaller conspecifics offer abundant feeding opportunities, and where
alternative preys are difficult to find.
Acknowledgements We thank Team Bufo and the staff of Beatrice
Hill Farm for support and encouragement, Barry Scott (Parks and
Wildlife Commission of the Northern Territory) and the Northern
Territory Lands Corporation for access to laboratory facilities, Greg
Brown for unpublished data, and Mattias Hagman and especially
Travis Child for stimulating our interest in cannibalism in toads and
for many discussions. Christa Beckmann, Michael Crossland, and
Matt Greenlees helped with fieldwork, Christa Beckmann took some
of the photographs, and the Australian Research Council (RS) and
CAPES (LP) provided financial support. All procedures were
approved by the University of Sydney Animal Ethics Committee
(approval L04/5-2007/3/4515).
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